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Microbiome analysis in Lascaux Cave in relation to black stain alterations of rock surfaces and collembola.

ABSTRACT: Anthropization of Palaeolithic caves open for tourism may favour collembola invasion and result in the formation of black stains attributed to pigmented fungi. However, ecological processes underpinning black stain formation are not fully understood. Here, we tested the hypotheses that black stains from the Apse room of Lascaux Cave display a specific microbiota enriched in pigmented fungi, and that collembola thriving on the stains have the potential to consume and disseminate these black fungi. Metabarcoding showed that the microbiota of black stains and neighbouring unstained parts strongly differed, with in black stains a higher prevalence of Ochroconis and other pigmented fungi and the strong regression of Pseudomonas bacteria (whose isolates inhibited in vitro the growth of pigmented fungi). Isotopic analyses indicated that Folsomia candida collembola thriving on stains could feed on black stain in situ and assimilate the pigmented fungi they were fed with in vitro. They could carry these fungi and disseminate them when tested with complex black stains from Lascaux. This shows that black stain formation is linked to the development of pigmented fungi, which coincides with the elimination of antagonistic pseudomonads, and points towards a key role of F. candida collembola in the dynamics of pigmented fungi.

SUBMITTER: Alonso L

PROVIDER: S-EPMC10103860 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Microbiome analysis in Lascaux Cave in relation to black stain alterations of rock surfaces and collembola.

Alonso Lise L Pommier Thomas T Simon Laurent L Maucourt Flavien F Doré Jeanne J Dubost Audrey A Trân Van Van V Minard Guillaume G Valiente Moro Claire C Douady Christophe J CJ Moënne-Loccoz Yvan Y

Environmental microbiology reports 20221124 2

Anthropization of Palaeolithic caves open for tourism may favour collembola invasion and result in the formation of black stains attributed to pigmented fungi. However, ecological processes underpinning black stain formation are not fully understood. Here, we tested the hypotheses that black stains from the Apse room of Lascaux Cave display a specific microbiota enriched in pigmented fungi, and that collembola thriving on the stains have the potential to consume and disseminate these black fungi ...[more]

PMID: 36424842

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Project description:BackgroundThe World-famous UNESCO heritage from the Paleolithic human society, Lascaux Cave (France), has endeavored intense microclimatic perturbations, in part due to high touristic pressure. These perturbations have resulted in numerous disturbances of the cave ecosystem, including on its microbial compartment, which resulted in the formation of black stains especially on the rock faces of the passage. We investigated the cave microbiome in this part of Lascaux by sampling three mineral substrates (soil, banks, and inclined planes) on and outside stains to assess current cave microbial assemblage and explore the possibility that pigmented microorganisms involved in stain development occur as microbial consortia.MethodsMicrobial abundance and diversity were assessed by means of quantitative PCR and high-throughput sequencing (Illumina MiSeq) of several DNA and cDNA taxonomic markers. Five sampling campaigns were carried out during winter and summer to embrace potential seasonal effect in this somewhat stable environment (based on measurements of temperature and CO2 concentration).ResultsWhile the season or type of mineral substrate did not affect the abundances of bacteria and micro-eukaryotes on or outside stains, mineral substrate rather than stain presence appears to be the most significant factor determining microbial diversity and structuring microbial community, regardless of whether DNA or cDNA markers were considered. A phylogenetic signal was also detected in relation to substrate types, presence of stains but not with season among the OTUs common to the three substrates. Co-occurrence network analyses showed that most bacterial and fungal interactions were positive regardless of the factor tested (season, substrate, or stain), but these networks varied according to ecological conditions and time. Microorganisms known to harbor pigmentation ability were well established inside but also outside black stains, which may be prerequisite for subsequent stain formation.ConclusionsThis first high throughput sequencing performed in Lascaux Cave showed that black stains were secondary to mineral substrate in determining microbiome community structure, regardless of whether total or transcriptionally active bacterial and micro-eukaryotic communities were considered. These results revealed the potential for new stain formation and highlight the need for careful microbiome management to avoid further cave wall degradation.

Project description:BackgroundCave anthropization related to rock art tourism can lead to cave microbiota imbalance and microbial alterations threatening Paleolithic artwork, but the underpinning microbial changes are poorly understood. Caves can be microbiologically heterogeneous and certain rock wall alterations may develop in different rooms despite probable spatial heterogeneity of the cave microbiome, suggesting that a same surface alteration might involve a subset of cosmopolitan taxa widespread in each cave room. We tested this hypothesis in Lascaux, by comparing recent alterations (dark zones) and nearby unmarked surfaces in nine locations within the cave.ResultsIllumina MiSeq metabarcoding of unmarked surfaces confirmed microbiome heterogeneity of the cave. Against this background, the microbial communities of unmarked and altered surfaces differed at each location. The use of a decision matrix showed that microbiota changes in relation to dark zone formation could differ according to location, but dark zones from different locations displayed microbial similarities. Thus, dark zones harbor bacterial and fungal taxa that are cosmopolitan at the scale of Lascaux, as well as dark zone-specific taxa present (i) at all locations in the cave (i.e. the six bacterial genera Microbacterium, Actinophytocola, Lactobacillus, Bosea, Neochlamydia and Tsukamurella) or (ii) only at particular locations within Lascaux. Scanning electron microscopy observations and most qPCR data evidenced microbial proliferation in dark zones.ConclusionFindings point to the proliferation of different types of taxa in dark zones, i.e. Lascaux-cosmopolitan bacteria and fungi, dark zone-specific bacteria present at all locations, and dark zone-specific bacteria and fungi present at certain locations only. This probably explains why dark zones could form in various areas of the cave and suggests that the spread of these alterations might continue according to the area of distribution of key widespread taxa.

Project description:ObjectiveTo assess the epidemiologic attributes and microbial variations associated with extrinsic black tooth stain (BTS) among Chinese preschool children.MethodsThis cross-sectional study included 250 preschool children (3-4 years) from three kindergartens in Shanghai, China. Following clinical examination, and using a case-control design, saliva and dental plaque specimens were collected from caries-free participants with (n = 21, BTS group) and without (n = 48, control group) BTS. The chi-square test and logistic regression model were used to evaluate factors associated with BTS. 16S rRNA sequencing were used to characterize the associated microbial communities.ResultsBTS was detected in 12.4% of participants, with a mean of 13.7 black-stained teeth. Participants with BTS had a lower caries burden and better oral hygiene (P = 0.003). Children with less frequent intake of marmalade or honey (P = 0.033) and regular application of fluoride (P = 0.007) had a lower likelihood of having BTS. Microbiota analysis revealed 14 phyla, 35 classes, 63 orders, 113 families, 221 genera, 452 species, and 1,771 operational taxonomic units (OTUs). In terms of microbial diversity, no significant differences were observed in the saliva of the two groups (P > 0.05). Dental plaque from the BTS group exhibited higher OTU richness but lower evenness than that from the control group (Chao P = 0.006, Shannon P = 0.007, respectively) and showed a significant difference in β diversity (P = 0.002). The microbiome in the two groups was characterized by various microbial biomarkers, such as Pseudomonas fluorescens, Leptotrichia sp._HMT_212, Actinomyces sp._HMT_169, and Aggregatibacter sp._HMT_898 in plaques from the BTS group. Functional analysis of the microbial species suggested the existence of a hyperactive metabolic state on teeth surfaces with BTS plaques and revealed that ferric iron, the iron complex transport system, and the iron (III) transport system were more abundant in BTS plaque samples.ConclusionsThis study provides insights into the epidemiologic and microbial features of BTS in preschool children. The microbiome in BTS is characterized by various microbial biomarkers, which can serve as indicators for BTS diagnosis and prognosis.

Project description:IntroductionA lower prevalence of dental caries (hereafter termed "caries") has been observed in children with dental extrinsic black stain (EBS).MethodsWe investigated the epidemiologic characterization of EBS and explored the possible role of the oral microbiome (OM) and gut microbiome (GM) in EBS formation and caries prevention. In an epidemiologic survey, 2,675 children aged 3-6 years were included. Thirty-eight of these children (7 children had both caries and EBS, 10 had EBS only, 11 had caries only, and 10 were healthy children) were recruited for 16S rRNA sequencing and collection of samples of supragingival plaque and feces. Collected plaque samples were divided into four groups: BCP (EBS+, caries+), BP (EBS+, caries-), CP (EBS-, caries+), and P (EBS-, caries-). Fecal samples were also divided into four groups: BCF (EBS+, caries+), BF (EBS+, caries-), CF (EBS-, caries+), and F (EBS-, caries-).ResultsEBS was observed in 12.10% of this population. Children with EBS had a significantly reduced prevalence of caries and a lower mean value of decayed-missing-filled teeth (dmft; p < 0.01). According to analyses of dental plaque, the P group had the most complex microbiome. The BCP group exhibited greater operational taxonomic unit (OTU) richness but a reduced evenness compared with the BP group, and the CP group showed greater OTU richness than the BP group. At the genus level, higher abundance of Actinomyces and Cardiobacterium species was observed in the BCP group. Higher abundance of Lautropia and Pesudopropionibacteriumin species was observed in the BP group compared with P and CP groups, respectively (p < 0.05). Veillonella species were significantly more common in P and CP groups than in BP groups, whereas Porphyromonas and Fusobacterium species were more common in the CP group (p < 0.05). With regard to the GM, the CF group exhibited greater OTU diversity than the BF group. The GM in the BCF group exhibited the most complex relationships across all fecal groups. GM groups could be distinguished by various unique biomarkers, such as Escherichia and Shigella species in the BCF group, Agathobacter and Ruminococcus species in the CF group, Lactobacillus species in the BF group, and Roseburia species in the F group. Our results suggest that EBS is a possible protective factor against early-childhood caries. Dental plaque and the GM may be relevant to EBS in primary dentition.

Dataset Information

Microbiome analysis in Lascaux Cave in relation to black stain alterations of rock surfaces and collembola.

Publications

Microbiome analysis in Lascaux Cave in relation to black stain alterations of rock surfaces and collembola.

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